Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Profiling bovine blastocyst microRNAs using deep sequencing

R. Pasquariello A G , B. Fernandez-Fuertes B , F. Strozzi C , F. Pizzi D , R. Mazza E , P. Lonergan B , F. Gandolfi A and J. L. Williams F
+ Author Affiliations
- Author Affiliations

A Dipartimento di Scienze Agrarie e Ambientali – Produzione, Territori, Università degli Studi di Milano, Via Celoria 2, 20133, Milan, Italy.

B School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Dublin, Ireland.

C Parco Tecnologico Padano, Via Einstein Albert, 26900, Lodi, Italy.

D Istituto di Biologia e Biotecnologia Agraria – Consiglio Nazionale delle Ricerche, Via Einstein Albert, 26900, Lodi, Italy.

E Associazione Italiana Allevatori, Via Bergamo 292, 26100, Cremona, Italy.

F School of Animal and Veterinary Sciences, Faculty of Science, University of Adelaide, Roseworthy, SA 5371, Australia.

G Corresponding author. Email: rolando.pasquariello@libero.it

Reproduction, Fertility and Development 29(8) 1545-1555 https://doi.org/10.1071/RD16110
Submitted: 8 March 2016  Accepted: 24 June 2016   Published: 13 September 2016

Abstract

MicroRNAs (miRNAs) are known to control several reproductive functions, including oocyte maturation, implantation and early embryonic development. Recent advances in deep sequencing have allowed the analysis of all miRNAs of a sample. However, when working with embryos, due to the low RNA content, miRNA profiling is challenging because of the relatively large amount of total RNA required for library preparation protocols. In the present study we compared three different procedures for RNA extraction and prepared libraries using pools of 30 bovine blastocysts. In total, 14 of the 15 most abundantly expressed miRNAs were common to all three procedures. Furthermore, using miRDeep discovery and annotation software (Max Delbrück Center), we identified 1363 miRNA sequences, of which bta-miR-10b and bta-miR-378 were the most abundant. Most of the 179 genes identified as experimentally validated (86.6%) or predicted targets (13.4%) were associated with cancer canonical pathways. We conclude that reliable analysis of bovine blastocyst miRNAs can be achieved using the procedures described herein. The repeatability of the results across different procedures and independent replicates, as well as their consistency with results obtained in other species, support the biological relevance of these miRNAs and of the gene pathways they modulate in early embryogenesis.

Additional keywords: epigenetics, gene regulation, RNA.


References

Abd El Naby, W. S., Hagos, T. H., Hossain, M. M., Salilew-Wondim, D., Gad, A. Y., Rings, F., Cinar, M. U., Tholen, E., Looft, C., Schellander, K., Hoelker, M., and Tesfaye, D. (2013). Expression analysis of regulatory microRNAs in bovine cumulus oocyte complex and preimplantation embryos. Zygote 21, 31–51.
Expression analysis of regulatory microRNAs in bovine cumulus oocyte complex and preimplantation embryos.CrossRef | 1:CAS:528:DC%2BC3sXhsVamtb4%3D&md5=e650ad0da628743113b224f9cab99c3cCAS | 22008281PubMed | open url image1

Bar, M., Wyman, S. K., Fritz, B. R., Qi, J., Garg, K. S., Parkin, R. K., Kroh, E. M., Bendoraite, A., Mitchell, P. S., Nelson, A. M., Ruzzo, W. L., Ware, C., Radich, J. P., Gentleman, R., Ruohola-Baker, H., and Tewari, M. (2008). MicroRNA discovery and profiling in human embryonic stem cells by deep sequencing of small RNA libraries. Stem Cells 26, 2496–2505.
MicroRNA discovery and profiling in human embryonic stem cells by deep sequencing of small RNA libraries.CrossRef | 1:CAS:528:DC%2BD1cXhtlyku7rP&md5=ce592ba36cd35966693b2539543ed2c8CAS | 18583537PubMed | open url image1

Betoni, J. S., Derr, K., Pahl, M. C., Rogers, L., Muller, C. L., Packard, R. E., Carey, D. J., Kuivaniemi, H., and Tromp, G. (2013). MicroRNA analysis in placentas from patients with preeclampsia: comparison of new and published results. Hypertens. Pregnancy 32, 321–339.
MicroRNA analysis in placentas from patients with preeclampsia: comparison of new and published results.CrossRef | 1:CAS:528:DC%2BC3sXhsFerurrE&md5=b8bb860caf860dfee439d82e9b1c4314CAS | 23844600PubMed | open url image1

Braga, D. P., Setti, A. S., Figueira, R. C., Iaconelli, A., and Borges, E. (2014). The importance of the cleavage stage morphology evaluation for blastocyst transfer in patients with good prognosis. J. Assist. Reprod. Genet. 31, 1105–1110.
The importance of the cleavage stage morphology evaluation for blastocyst transfer in patients with good prognosis.CrossRef | 24893729PubMed | open url image1

Calin, G. A., Ferracin, M., Cimmino, A., Di Leva, G., Shimizu, M., Wojcik, S. E., Iorio, M. V., Visone, R., Sever, N. I., Fabbri, M., Iuliano, R., Palumbo, T., Pichiorri, F., Roldo, C., Garzon, R., Sevignani, C., Rassenti, L., Alder, H., Volinia, S., Liu, C. G., Kipps, T. J., Negrini, M., and Croce, C. M. (2005). A microRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N. Engl. J. Med. 353, 1793–1801.
A microRNA signature associated with prognosis and progression in chronic lymphocytic leukemia.CrossRef | 1:CAS:528:DC%2BD2MXhtFKrtLbJ&md5=68645bd2ef133ebbaedd399e664e1604CAS | 16251535PubMed | open url image1

Carolan, C., Lonergan, P., Van Langendonckt, A., and Mermillod, P. (1995). Factors affecting bovine embryo development in synthetic oviduct fluid following oocyte maturation and fertilization in vitro. Theriogenology 43, 1115–1128.
Factors affecting bovine embryo development in synthetic oviduct fluid following oocyte maturation and fertilization in vitro.CrossRef | 1:STN:280:DC%2BD28zgtVCmtw%3D%3D&md5=d419e90c319ed0fd2da66dd599d7be0cCAS | 16727698PubMed | open url image1

Chim, S. S., Shing, T. K., Hung, E. C., Leung, T. Y., Lau, T. K., Chiu, R. W., and Lo, Y. M. (2008). Detection and characterization of placental microRNAs in maternal plasma. Clin. Chem. 54, 482–490.
Detection and characterization of placental microRNAs in maternal plasma.CrossRef | 1:CAS:528:DC%2BD1cXivVansrc%3D&md5=fcc62624cced015d391f65b7ca239a66CAS | 18218722PubMed | open url image1

Chitwood, J. L., Rincon, G., Kaiser, G. G., Medrano, J. F., and Ross, P. J. (2013). RNA-seq analysis of single bovine blastocysts. BMC Genomics 14, 350.
RNA-seq analysis of single bovine blastocysts.CrossRef | 1:CAS:528:DC%2BC3sXpslyisrs%3D&md5=2ea4f7838c661e12e9005434bcd23162CAS | 23705625PubMed | open url image1

Cimmino, A., Calin, G. A., Fabbri, M., Iorio, M. V., Ferracin, M., Shimizu, M., Wojcik, S. E., Aqeilan, R. I., Zupo, S., Dono, M., Rassenti, L., Alder, H., Volinia, S., Liu, C. G., Kipps, T. J., Negrini, M., and Croce, C. M. (2005). miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc. Natl Acad. Sci. USA 102, 13 944–13 949.
miR-15 and miR-16 induce apoptosis by targeting BCL2.CrossRef | 1:CAS:528:DC%2BD2MXhtVOqsbjK&md5=8f2440059e32984662559ca3cabeb8d1CAS | open url image1

Cleys, E. R., Halleran, J. L., McWhorter, E., Hergenreder, J., Enriquez, V. A., da Silveira, J. C., Bruemmer, J. E., Winger, Q. A., and Bouma, G. J. (2014). Identification of microRNAs in exosomes isolated from serum and umbilical cord blood, as well as placentomes of gestational day 90 pregnant sheep. Mol. Reprod. Dev. 81, 983–993.
Identification of microRNAs in exosomes isolated from serum and umbilical cord blood, as well as placentomes of gestational day 90 pregnant sheep.CrossRef | 1:CAS:528:DC%2BC2cXhvVykt77K&md5=93551972649180218a5206f31ddf6efdCAS | 25269776PubMed | open url image1

Coutinho, L. L., Matukumalli, L. K., Sonstegard, T. S., Van Tassell, C. P., Gasbarre, L. C., Capuco, A. V., and Smith, T. P. (2007). Discovery and profiling of bovine microRNAs from immune-related and embryonic tissues. Physiol. Genomics 29, 35–43.
Discovery and profiling of bovine microRNAs from immune-related and embryonic tissues.CrossRef | 1:CAS:528:DC%2BD2sXktVaru7s%3D&md5=1db55aa34732d3755236d4119413a17eCAS | 17105755PubMed | open url image1

Dennis, G., Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H. C., and Lempicki, R. A. (2003). DAVID: database for annotation, visualization, and integrated discovery. Genome Biol. 4, P3.
DAVID: database for annotation, visualization, and integrated discovery.CrossRef | 12734009PubMed | open url image1

Du, Y., Wang, X., Wang, B., Chen, W., He, R., Zhang, L., Xing, X., Su, J., Wang, Y., and Zhang, Y. (2014). Deep sequencing analysis of microRNAs in bovine sperm. Mol. Reprod. Dev. 81, 1042–1052.
Deep sequencing analysis of microRNAs in bovine sperm.CrossRef | 1:CAS:528:DC%2BC2cXhvVykt7%2FN&md5=85e0a5400543da586a3867362422a291CAS | 25279827PubMed | open url image1

Feng, R., Sang, Q., Zhu, Y., Fu, W., Liu, M., Xu, Y., Shi, H., Xu, Y., Qu, R., Chai, R., Shao, R., Jin, L., He, L., Sun, X., and Wang, L. (2015). MiRNA-320 in the human follicular fluid is associated with embryo quality in vivo and affects mouse embryonic development in vitro. Sci. Rep. 5, 8689.
MiRNA-320 in the human follicular fluid is associated with embryo quality in vivo and affects mouse embryonic development in vitro.CrossRef | 1:CAS:528:DC%2BC2MXhtFKhtbvL&md5=539a46a23e392851fe75534c28bf1da4CAS | 25732513PubMed | open url image1

Fkih M’hamed, I., Privat, M., Ponelle, F., Penault-Llorca, F., Kenani, A., and Bignon, Y. J. (2015). Identification of miR-10b, miR-26a, miR-146a and miR-153 as potential triple-negative breast cancer biomarkers. Cell Oncol. (Dordr.) 38, 433–442.
Identification of miR-10b, miR-26a, miR-146a and miR-153 as potential triple-negative breast cancer biomarkers.CrossRef | 1:CAS:528:DC%2BC2MXhsFyru77L&md5=46f93583f6113c05e007719b15ef05bfCAS | 26392359PubMed | open url image1

Fomeshi, M. R., Ebrahimi, M., Mowla, S. J., Khosravani, P., Firouzi, J., and Khayatzadeh, H. (2015). Evaluation of the expressions pattern of miR-10b, 21, 200c, 373 and 520c to find the correlation between epithelial-to-mesenchymal transition and melanoma stem cell potential in isolated cancer stem cells. Cell. Mol. Biol. Lett. 20, 448–465.
Evaluation of the expressions pattern of miR-10b, 21, 200c, 373 and 520c to find the correlation between epithelial-to-mesenchymal transition and melanoma stem cell potential in isolated cancer stem cells.CrossRef | 1:CAS:528:DC%2BC2MXht1Ogu7jO&md5=d46323b9b41a8382fa738b381a9ea223CAS | 26208390PubMed | open url image1

Frankel, L. B., Christoffersen, N. R., Jacobsen, A., Lindow, M., Krogh, A., and Lund, A. H. (2008). Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. J. Biol. Chem. 283, 1026–1033.
Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells.CrossRef | 1:CAS:528:DC%2BD1cXhsFaktw%3D%3D&md5=25ce4b196351d23d6fea4533beb88383CAS | 17991735PubMed | open url image1

Friedländer, M. R., Mackowiak, S. D., Li, N., Chen, W., and Rajewsky, N. (2012). miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Res. 40, 37–52.
miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades.CrossRef | 21911355PubMed | open url image1

Galli, C., Duchi, R., Colleoni, S., Lagutina, I., and Lazzari, G. (2014). Ovum pick up, intracytoplasmic sperm injection and somatic cell nuclear transfer in cattle, buffalo and horses: from the research laboratory to clinical practice. Theriogenology 81, 138–151.
Ovum pick up, intracytoplasmic sperm injection and somatic cell nuclear transfer in cattle, buffalo and horses: from the research laboratory to clinical practice.CrossRef | 24274418PubMed | open url image1

Galliano, D., and Pellicer, A. (2014). MicroRNA and implantation. Fertil. Steril. 101, 1531–1544.
MicroRNA and implantation.CrossRef | 1:CAS:528:DC%2BC2cXpvFGiurk%3D&md5=6526457026f47fea10e9c1c4ed8326d3CAS | 24882617PubMed | open url image1

Garzon, R., Volinia, S., Liu, C. G., Fernandez-Cymering, C., Palumbo, T., Pichiorri, F., Fabbri, M., Coombes, K., Alder, H., Nakamura, T., Flomenberg, N., Marcucci, G., Calin, G. A., Kornblau, S. M., Kantarjian, H., Bloomfield, C. D., Andreeff, M., and Croce, C. M. (2008a). MicroRNA signatures associated with cytogenetics and prognosis in acute myeloid leukemia. Blood 111, 3183–3189.
MicroRNA signatures associated with cytogenetics and prognosis in acute myeloid leukemia.CrossRef | 1:CAS:528:DC%2BD1cXjvVamtbY%3D&md5=79ecb129fe97e5cb72b5081c7c7a0349CAS | 18187662PubMed | open url image1

Garzon, R., Garofalo, M., Martelli, M. P., Briesewitz, R., Wang, L., Fernandez-Cymering, C., Volinia, S., Liu, C. G., Schnittger, S., Haferlach, T., Liso, A., Diverio, D., Mancini, M., Meloni, G., Foa, R., Martelli, M. F., Mecucci, C., Croce, C. M., and Falini, B. (2008b). Distinctive miRNA signature of acute myeloid leukemia bearing cytoplasmic mutated nucleophosmin. Proc. Natl Acad. Sci. USA 105, 3945–3950.
Distinctive miRNA signature of acute myeloid leukemia bearing cytoplasmic mutated nucleophosmin.CrossRef | 1:CAS:528:DC%2BD1cXjs1OgtLw%3D&md5=ef555766f6d78b833a08caaf70bc751cCAS | 18308931PubMed | open url image1

Gebremedhn, S., Salilew-Wondim, D., Ahmad, I., Sahadevan, S., Hossain, M. M., Hoelker, M., Rings, F., Neuhoff, C., Tholen, E., Looft, C., Schellander, K., and Tesfaye, D. (2015). MicroRNA expression profile in bovine granulosa cells of preovulatory dominant and subordinate follicles during the late follicular phase of the estrous cycle. PLoS One 10, e0125912.
MicroRNA expression profile in bovine granulosa cells of preovulatory dominant and subordinate follicles during the late follicular phase of the estrous cycle.CrossRef | 25993098PubMed | open url image1

Gilchrist, G. C., Tscherner, A., Nalpathamkalam, T., Merico, D., and LaMarre, J. (2016). MicroRNA expression during bovine oocyte maturation and fertilization. Int. J. Mol. Sci. 17, 396.
MicroRNA expression during bovine oocyte maturation and fertilization.CrossRef | 26999121PubMed | open url image1

Goossens, K., De Spiegelaere, W., Stevens, M., Burvenich, C., De Spiegeleer, B., Cornillie, P., Van Zeveren, A., Van Soom, A., and Peelman, L. (2012). Differential microRNA expression analysis in blastocysts by whole mount in situ hybridization and reverse transcription quantitative polymerase chain reaction on laser capture microdissection samples. Anal. Biochem. 423, 93–101.
Differential microRNA expression analysis in blastocysts by whole mount in situ hybridization and reverse transcription quantitative polymerase chain reaction on laser capture microdissection samples.CrossRef | 1:CAS:528:DC%2BC38XjsFOnu7o%3D&md5=b0b350c5afc3e6d7bb88b9a294dd71a1CAS | 22306474PubMed | open url image1

Goossens, K., Mestdagh, P., Lefever, S., Van Poucke, M., Van Zeveren, A., Van Soom, A., Vandesompele, J., and Peelman, L. (2013). Regulatory microRNA network identification in bovine blastocyst development. Stem Cells Dev. 22, 1907–1920.
Regulatory microRNA network identification in bovine blastocyst development.CrossRef | 1:CAS:528:DC%2BC3sXpslCiu7Y%3D&md5=5ab005a937afe04daba24621d01c4bf3CAS | 23398486PubMed | open url image1

Goossens, K., Peelman, L., and Van Soom, A. (2014). MicroRNA in situ hybridization on whole-mount preimplantation embryos. Methods Mol. Biol. 1211, 15–25.
MicroRNA in situ hybridization on whole-mount preimplantation embryos.CrossRef | 1:CAS:528:DC%2BC2MXotlOhtr4%3D&md5=835fa92e9ca3e5d7f86ef3b9f8367ba8CAS | 25218373PubMed | open url image1

Imbar, T., Galliano, D., Pellicer, A., and Laufer, N. (2014). Introduction: MicroRNAs in human reproduction: small molecules with crucial regulatory roles. Fertil. Steril. 101, 1514–1515.
Introduction: MicroRNAs in human reproduction: small molecules with crucial regulatory roles.CrossRef | 24882615PubMed | open url image1

Jiang, J., and Hui, C. C. (2008). Hedgehog signaling in development and cancer. Dev. Cell 15, 801–812.
Hedgehog signaling in development and cancer.CrossRef | 1:CAS:528:DC%2BD1cXhsFWgsbjN&md5=33b21c6d6f71d0089c16a3ead0bd2b05CAS | 19081070PubMed | open url image1

Jin, Y., Lu, J., Wen, J., Shen, Y., and Wen, X. (2015). Regulation of growth of human bladder cancer by miR-192. Tumour Biol. 36, 3791–3797.
Regulation of growth of human bladder cancer by miR-192.CrossRef | 1:CAS:528:DC%2BC2MXhtVCrtL4%3D&md5=a648d55f5ae2a79c19c87d8fd212d99eCAS | 25566965PubMed | open url image1

Kambe, S., Yoshitake, H., Yuge, K., Ishida, Y., Ali, M. M., Takizawa, T., Kuwata, T., Ohkuchi, A., Matsubara, S., Suzuki, M., Takeshita, T., Saito, S., and Takizawa, T. (2014). Human exosomal placenta-associated miR-517a-3p modulates the expression of PRKG1 mRNA in Jurkat cells. Biol. Reprod. 91, 129.
Human exosomal placenta-associated miR-517a-3p modulates the expression of PRKG1 mRNA in Jurkat cells.CrossRef | 25273530PubMed | open url image1

Kang, J. T., Atikuzzaman, M., Kwon, D. K., Park, S. J., Kim, S. J., Moon, J. H., Koo, O. J., Jang, G., and Lee, B. C. (2012). Developmental competence of porcine oocytes after in vitro maturation and in vitro culture under different oxygen concentrations. Zygote 20, 1–8.
Developmental competence of porcine oocytes after in vitro maturation and in vitro culture under different oxygen concentrations.CrossRef | 1:CAS:528:DC%2BC38Xjs1arug%3D%3D&md5=57ce80ab1a5e168d7f9c34ca1c783e0aCAS | 21791162PubMed | open url image1

Kang, Y. J., Lees, M., Matthews, L. C., Kimber, S. J., Forbes, K., and Aplin, J. D. (2015). MiR-145 suppresses embryo–epithelial juxtacrine communication at implantation by modulating maternal IGF1R. J. Cell Sci. 128, 804–814.
MiR-145 suppresses embryo–epithelial juxtacrine communication at implantation by modulating maternal IGF1R.CrossRef | 1:CAS:528:DC%2BC2MXmtlSitr8%3D&md5=abfa3d86ddeac109450ef1306fa72f24CAS | 25609710PubMed | open url image1

Karube, Y., Tanaka, H., Osada, H., Tomida, S., Tatematsu, Y., Yanagisawa, K., Yatabe, Y., Takamizawa, J., Miyoshi, S., Mitsudomi, T., and Takahashi, T. (2005). Reduced expression of Dicer associated with poor prognosis in lung cancer patients. Cancer Sci. 96, 111–115.
Reduced expression of Dicer associated with poor prognosis in lung cancer patients.CrossRef | 1:CAS:528:DC%2BD2MXislOhs7g%3D&md5=5dcadd6dcf5f21e228d75ca6217e439fCAS | 15723655PubMed | open url image1

Kozomara, A., and Griffiths-Jones, S. (2014). miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 42, D68–D73.
miRBase: annotating high confidence microRNAs using deep sequencing data.CrossRef | 1:CAS:528:DC%2BC2cXos1Wk&md5=7391794021fb3c9fa2fc8c2431316780CAS | 24275495PubMed | open url image1

Kridli, R. T., Khalaj, K., Bidarimath, M., and Tayade, C. (2016). Placentation, maternal–fetal interface, and conceptus loss in swine. Theriogenology 85, .
Placentation, maternal–fetal interface, and conceptus loss in swine.CrossRef | 1:CAS:528:DC%2BC2MXhtlOmt7jP&md5=f1228a77188c8e6b2ec65bc4bb3fc9aeCAS | 26324112PubMed | open url image1

Kropp, J., and Khatib, H. (2015). Characterization of microRNA in bovine in vitro culture media associated with embryo quality and development. J. Dairy Sci. 98, 6552–6563.
Characterization of microRNA in bovine in vitro culture media associated with embryo quality and development.CrossRef | 1:CAS:528:DC%2BC2MXhtFehsL7P&md5=8ba33dce67938c37af37c51541d4d11bCAS | 26142856PubMed | open url image1

Kropp, J., Salih, S. M., and Khatib, H. (2014). Expression of microRNAs in bovine and human pre-implantation embryo culture media. Front. Genet. 5, 91.
Expression of microRNAs in bovine and human pre-implantation embryo culture media.CrossRef | 24795753PubMed | open url image1

Li, G., Cai, M., Fu, D., Chen, K., Sun, M., Cai, Z., and Cheng, B. (2012). Heat shock protein 90B1 plays an oncogenic role and is a target of microRNA-223 in human osteosarcoma. Cell. Physiol. Biochem. 30, 1481–1490.
Heat shock protein 90B1 plays an oncogenic role and is a target of microRNA-223 in human osteosarcoma.CrossRef | 1:CAS:528:DC%2BC3sXhslWitrk%3D&md5=d68ec7892061a98a4bac6107782475a8CAS | 23208072PubMed | open url image1

Li, Y., Fang, Y., Liu, Y., and Yang, X. (2015a). MicroRNAs in ovarian function and disorders. J. Ovarian Res. 8, 51.
MicroRNAs in ovarian function and disorders.CrossRef | 26232057PubMed | open url image1

Li, Z., Jia, J., Gou, J., Tong, A., Liu, X., Zhao, X., and Yi, T. (2015b). Mmu-miR-126a-3p plays a role in murine embryo implantation by regulating Itga11. Reprod. Biomed. Online 31, 384–393.
Mmu-miR-126a-3p plays a role in murine embryo implantation by regulating Itga11.CrossRef | 1:CAS:528:DC%2BC2MXhtVeksLvK&md5=48e161c1a6225bfac8f3dc157538f3e0CAS | 26194885PubMed | open url image1

Liang, X., Liu, Y., Mei, S., Zhang, M., Xin, J., Zhang, Y., and Yang, R. (2015). MicroRNA-22 impairs anti-tumor ability of dendritic cells by targeting p38. PLoS One 10, e0121510.
MicroRNA-22 impairs anti-tumor ability of dendritic cells by targeting p38.CrossRef | 25826372PubMed | open url image1

Marzi, M. J., Puggioni, E. M., Dall’Olio, V., Bucci, G., Bernard, L., Bianchi, F., Crescenzi, M., Di Fiore, P. P., and Nicassio, F. (2012). Differentiation-associated microRNAs antagonize the Rb-E2F pathway to restrict proliferation. J. Cell Biol. 199, 77–95.
Differentiation-associated microRNAs antagonize the Rb-E2F pathway to restrict proliferation.CrossRef | 1:CAS:528:DC%2BC38XhsV2it73M&md5=693ce7e2c769fd5d944f0e0f1fd80df1CAS | 23027903PubMed | open url image1

McCallie, B. R., Parks, J. C., Strieby, A. L., Schoolcraft, W. B., and Katz-Jaffe, M. G. (2014). Human blastocysts exhibit unique microrna profiles in relation to maternal age and chromosome constitution. J. Assist. Reprod. Genet. 31, 913–919.
Human blastocysts exhibit unique microrna profiles in relation to maternal age and chromosome constitution.CrossRef | 24760722PubMed | open url image1

McManus, M. T. (2003). MicroRNAs and cancer. Semin. Cancer Biol. 13, 253–258.
MicroRNAs and cancer.CrossRef | 1:CAS:528:DC%2BD3sXntFykurY%3D&md5=b6b53dd67ac0e27b2fc3fb2f025beaa1CAS | 14563119PubMed | open url image1

Mitchell, M. D., Peiris, H. N., Kobayashi, M., Koh, Y. Q., Duncombe, G., Illanes, S. E., Rice, G. E., and Salomon, C. (2015). Placental exosomes in normal and complicated pregnancy. Am. J. Obstet. Gynecol. 213, S173–S181.
Placental exosomes in normal and complicated pregnancy.CrossRef | 1:CAS:528:DC%2BC28XhvFygtL8%3D&md5=cf2aee773795b546807123d3e073d559CAS | 26428497PubMed | open url image1

Mondou, E., Dufort, I., Gohin, M., Fournier, E., and Sirard, M. A. (2012). Analysis of microRNAs and their precursors in bovine early embryonic development. Mol. Hum. Reprod. 18, 425–434.
Analysis of microRNAs and their precursors in bovine early embryonic development.CrossRef | 1:CAS:528:DC%2BC38XhtlWmur3L&md5=e86b0dfd9006ee489f2c4ec366f4159dCAS | 22491901PubMed | open url image1

Monk, M., and Holding, C. (2001). Human embryonic genes re-expressed in cancer cells. Oncogene 20, 8085–8091.
Human embryonic genes re-expressed in cancer cells.CrossRef | 1:CAS:528:DC%2BD3MXptlKktb8%3D&md5=e359d7f4fde42d2fa66ca74f37ab4e2eCAS | 11781821PubMed | open url image1

Murri, M., Insenser, M., Fernández-Durán, E., San-Millán, J. L., and Escobar-Morreale, H. F. (2013). Effects of polycystic ovary syndrome (PCOS), sex hormones, and obesity on circulating miRNA-21, miRNA-27b, miRNA-103, and miRNA-155 expression. J. Clin. Endocrinol. Metab. 98, E1835–E1844.
Effects of polycystic ovary syndrome (PCOS), sex hormones, and obesity on circulating miRNA-21, miRNA-27b, miRNA-103, and miRNA-155 expression.CrossRef | 1:CAS:528:DC%2BC3sXhsl2msrjL&md5=3d18e0106c379052c1a6f61b78507abfCAS | 24037889PubMed | open url image1

Nagaraj, N. S., and Datta, P. K. (2010). Targeting the transforming growth factor-beta signaling pathway in human cancer. Expert Opin. Investig. Drugs 19, 77–91.
Targeting the transforming growth factor-beta signaling pathway in human cancer.CrossRef | 1:CAS:528:DC%2BD1MXhsFCiu77J&md5=f9a25042c24b6e5f16a2bdbbd2fc59cfCAS | 20001556PubMed | open url image1

Nagpal, N., Ahmad, H. M., Chameettachal, S., Sundar, D., Ghosh, S., and Kulshreshtha, R. (2015). HIF-inducible miR-191 promotes migration in breast cancer through complex regulation of TGFβ-signaling in hypoxic microenvironment. Sci. Rep. 5, 9650.
HIF-inducible miR-191 promotes migration in breast cancer through complex regulation of TGFβ-signaling in hypoxic microenvironment.CrossRef | 1:CAS:528:DC%2BC2MXhtFOrsrnL&md5=e8ca24659d2495ee082fcdc00e418d30CAS | 25867965PubMed | open url image1

Nishida, N., Nagahara, M., Sato, T., Mimori, K., Sudo, T., Tanaka, F., Shibata, K., Ishii, H., Sugihara, K., Doki, Y., and Mori, M. (2012). Microarray analysis of colorectal cancer stromal tissue reveals upregulation of two oncogenic miRNA clusters. Clin. Cancer Res. 18, 3054–3070.
Microarray analysis of colorectal cancer stromal tissue reveals upregulation of two oncogenic miRNA clusters.CrossRef | 1:CAS:528:DC%2BC38XnvVOgtLY%3D&md5=e59ecab15f17520fdd102dea750109b8CAS | 22452939PubMed | open url image1

Nishioka, N., Inoue, K., Adachi, K., Kiyonari, H., Ota, M., Ralston, A., Yabuta, N., Hirahara, S., Stephenson, R. O., Ogonuki, N., Makita, R., Kurihara, H., Morin-Kensicki, E. M., Nojima, H., Rossant, J., Nakao, K., Niwa, H., and Sasaki, H. (2009). The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev. Cell 16, 398–410.
The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass.CrossRef | 1:CAS:528:DC%2BD1MXjs1ynsrw%3D&md5=9c7f38d72431e6e12aefecae8bdc6d1eCAS | 19289085PubMed | open url image1

O’Donnell, K. A., Wentzel, E. A., Zeller, K. I., Dang, C. V., and Mendell, J. T. (2005). c-Myc-regulated microRNAs modulate E2F1 expression. Nature 435, 839–843.
c-Myc-regulated microRNAs modulate E2F1 expression.CrossRef | 1:CAS:528:DC%2BD2MXkvVGgsLg%3D&md5=9cb95b56cdfdb05e57e8b00cd4fe3a38CAS | 15944709PubMed | open url image1

O’Hara, L., Forde, N., Kelly, A. K., and Lonergan, P. (2014). Effect of bovine blastocyst size at embryo transfer on Day 7 on conceptus length on Day 14: can supplementary progesterone rescue small embryos? Theriogenology 81, 1123–1128.
Effect of bovine blastocyst size at embryo transfer on Day 7 on conceptus length on Day 14: can supplementary progesterone rescue small embryos?CrossRef | 24582375PubMed | open url image1

Palacios, F., Abreu, C., Prieto, D., Morande, P., Ruiz, S., Fernández-Calero, T., Naya, H., Libisch, G., Robello, C., Landoni, A. I., Gabus, R., Dighiero, G., and Oppezzo, P. (2015). Activation of the PI3K/AKT pathway by microRNA-22 results in CLL B-cell proliferation. Leukemia 29, 115–125.
Activation of the PI3K/AKT pathway by microRNA-22 results in CLL B-cell proliferation.CrossRef | 1:CAS:528:DC%2BC2cXpsFekt7o%3D&md5=7fab101c64dc9e30a72c9feb6f8d42a9CAS | 24825182PubMed | open url image1

Pan, B., Toms, D., Shen, W., and Li, J. (2015). MicroRNA-378 regulates oocyte maturation via the suppression of aromatase in porcine cumulus cells. Am. J. Physiol. Endocrinol. Metab. 308, E525–E534.
MicroRNA-378 regulates oocyte maturation via the suppression of aromatase in porcine cumulus cells.CrossRef | 1:CAS:528:DC%2BC2MXls1CrtLY%3D&md5=a5426fd7e0de22a29e48fd888276bac1CAS | 25628423PubMed | open url image1

Pasqualini, L., Bu, H., Puhr, M., Narisu, N., Rainer, J., Schlick, B., Schäfer, G., Angelova, M., Trajanoski, Z., Börno, S. T., Schweiger, M. R., Fuchsberger, C., and Klocker, H. (2015). miR-22 and miR-29a are members of the androgen receptor cistrome modulating LAMC1 and Mcl-1 in prostate cancer. Mol. Endocrinol. 29, 1037–1054.
miR-22 and miR-29a are members of the androgen receptor cistrome modulating LAMC1 and Mcl-1 in prostate cancer.CrossRef | 1:CAS:528:DC%2BC2MXhtFykurrP&md5=df15239bc05f2f76e1fa9424cce31110CAS | 26052614PubMed | open url image1

Petrocca, F., Visone, R., Onelli, M. R., Shah, M. H., Nicoloso, M. S., de Martino, I., Iliopoulos, D., Pilozzi, E., Liu, C. G., Negrini, M., Cavazzini, L., Volinia, S., Alder, H., Ruco, L. P., Baldassarre, G., Croce, C. M., and Vecchione, A. (2008). E2F1-regulated microRNAs impair TGFβ-dependent cell cycle arrest and apoptosis in gastric cancer. Cancer Cell 13, 272–286.
E2F1-regulated microRNAs impair TGFβ-dependent cell cycle arrest and apoptosis in gastric cancer.CrossRef | 1:CAS:528:DC%2BD1cXjsVKgs7s%3D&md5=fa3c22f7dfb11d1ecc152cb5d0dc50feCAS | 18328430PubMed | open url image1

Ponsuksili, S., Tesfaye, D., Schellander, K., Hoelker, M., Hadlich, F., Schwerin, M., and Wimmers, K. (2014). Differential expression of miRNAs and their target mRNAs in endometria prior to maternal recognition of pregnancy associates with endometrial receptivity for in vivo- and in vitro-produced bovine embryos. Biol. Reprod. 91, 135.
Differential expression of miRNAs and their target mRNAs in endometria prior to maternal recognition of pregnancy associates with endometrial receptivity for in vivo- and in vitro-produced bovine embryos.CrossRef | 25253731PubMed | open url image1

Rayner, K. J., and Hennessy, E. J. (2013). Extracellular communication via microRNA: lipid particles have a new message. J. Lipid Res. 54, 1174–1181.
Extracellular communication via microRNA: lipid particles have a new message.CrossRef | 1:CAS:528:DC%2BC3sXlsFeksLg%3D&md5=e2dc059ddd8898c5c314fd74c4e9e07eCAS | 23505318PubMed | open url image1

Rizos, D., Ward, F., Duffy, P., Boland, M. P., and Lonergan, P. (2002). Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol. Reprod. Dev. 61, 234–248.
Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality.CrossRef | 1:CAS:528:DC%2BD38Xlt1Giug%3D%3D&md5=fd530554a4e416cc604ed66ebc4922a4CAS | 11803560PubMed | open url image1

Robinson, M. D., McCarthy, D. J., and Smyth, G. K. (2010). edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140.
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data.CrossRef | 1:CAS:528:DC%2BD1MXhs1WlurvO&md5=f460abb200a8b720c3960b07d113133cCAS | 19910308PubMed | open url image1

Rosenbluth, E. M., Shelton, D. N., Wells, L. M., Sparks, A. E., and Van Voorhis, B. J. (2014). Human embryos secrete microRNAs into culture media: a potential biomarker for implantation. Fertil. Steril. 101, 1493–1500.
Human embryos secrete microRNAs into culture media: a potential biomarker for implantation.CrossRef | 1:CAS:528:DC%2BC2cXksFWgurs%3D&md5=2ebfae343916492955cea19747f52860CAS | 24786747PubMed | open url image1

Salilew-Wondim, D., Ahmad, I., Gebremedhn, S., Sahadevan, S., Hossain, M. D., Rings, F., Hoelker, M., Tholen, E., Neuhoff, C., Looft, C., Schellander, K., and Tesfaye, D. (2014). The expression pattern of microRNAs in granulosa cells of subordinate and dominant follicles during the early luteal phase of the bovine estrous cycle. PLoS One 9, e106795.
The expression pattern of microRNAs in granulosa cells of subordinate and dominant follicles during the early luteal phase of the bovine estrous cycle.CrossRef | 25192015PubMed | open url image1

Sohel, M. M., Hoelker, M., Noferesti, S. S., Salilew-Wondim, D., Tholen, E., Looft, C., Rings, F., Uddin, M. J., Spencer, T. E., Schellander, K., and Tesfaye, D. (2013). Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid: implications for bovine oocyte developmental competence. PLoS One 8, e78505.
Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid: implications for bovine oocyte developmental competence.CrossRef | 1:CAS:528:DC%2BC3sXhslGisLjJ&md5=48d1c73f7d3de8b6134d507fb2898365CAS | 24223816PubMed | open url image1

Song, L., Liu, L., Wu, Z., Li, Y., Ying, Z., Lin, C., Wu, J., Hu, B., Cheng, S. Y., Li, M., and Li, J. (2012). TGF-β induces miR-182 to sustain NF-κB activation in glioma subsets. J. Clin. Invest. 122, 3563–3578.
TGF-β induces miR-182 to sustain NF-κB activation in glioma subsets.CrossRef | 1:CAS:528:DC%2BC38XhsV2itrfF&md5=43c3e83da0698a7d0e82b6c6aac796e2CAS | 23006329PubMed | open url image1

Song, J. L., Nigam, P., Tektas, S. S., and Selva, E. (2015). microRNA regulation of Wnt signaling pathways in development and disease. Cell. Signal. 27, 1380–1391.
microRNA regulation of Wnt signaling pathways in development and disease.CrossRef | 1:CAS:528:DC%2BC2MXmsF2hurw%3D&md5=d96dccfdb180a7df6c8790ce93ed4913CAS | 25843779PubMed | open url image1

Stowe, H. M., Calcatera, S. M., Dimmick, M. A., Andrae, J. G., Duckett, S. K., and Pratt, S. L. (2014). The bull sperm microRNAome and the effect of fescue toxicosis on sperm microRNA expression. PLoS One 9, e113163.
The bull sperm microRNAome and the effect of fescue toxicosis on sperm microRNA expression.CrossRef | 25462855PubMed | open url image1

Su, J., Liu, X., Sun, H., Wang, Y., Wu, Y., Guo, Z., and Zhang, Y. (2015). Identification of differentially expressed microRNAs in placentas of cloned and normally produced calves by Solexa sequencing. Anim. Reprod. Sci. 155, 64–74.
Identification of differentially expressed microRNAs in placentas of cloned and normally produced calves by Solexa sequencing.CrossRef | 1:CAS:528:DC%2BC2MXivFGqsLw%3D&md5=1c15e6c947fa0b103eb6a329ddb68281CAS | 25735829PubMed | open url image1

Toms, D., Xu, S., Pan, B., Wu, D., and Li, J. (2015). Progesterone receptor expression in granulosa cells is suppressed by microRNA-378-3p. Mol. Cell. Endocrinol. 399, 95–102.
Progesterone receptor expression in granulosa cells is suppressed by microRNA-378-3p.CrossRef | 1:CAS:528:DC%2BC2cXhsVKntLfP&md5=0fd6d50aa42201b6f5941ce5d0eb531dCAS | 25150622PubMed | open url image1

Tripurani, S. K., Xiao, C., Salem, M., and Yao, J. (2010). Cloning and analysis of fetal ovary microRNAs in cattle. Anim. Reprod. Sci. 120, 16–22.
Cloning and analysis of fetal ovary microRNAs in cattle.CrossRef | 1:CAS:528:DC%2BC3cXmtFWrtr0%3D&md5=51f45ec6d2550f1c7e8e90778cd6ca8fCAS | 20347535PubMed | open url image1

Tscherner, A., Gilchrist, G., Smith, N., Blondin, P., Gillis, D., and LaMarre, J. (2014). MicroRNA-34 family expression in bovine gametes and preimplantation embryos. Reprod. Biol. Endocrinol. 12, 85.
MicroRNA-34 family expression in bovine gametes and preimplantation embryos.CrossRef | 25179211PubMed | open url image1

Vlachos, I. S., Kostoulas, N., Vergoulis, T., Georgakilas, G., Reczko, M., Maragkakis, M., Paraskevopoulou, M. D., Prionidis, K., Dalamagas, T., and Hatzigeorgiou, A. G. (2012). DIANA miRPath v.2.0: investigating the combinatorial effect of microRNAs in pathways. Nucleic Acids Res. 40, W498–W504.
DIANA miRPath v.2.0: investigating the combinatorial effect of microRNAs in pathways.CrossRef | 1:CAS:528:DC%2BC3sXjtVCqs7Y%3D&md5=25651ee16204e8206ef441f7fac32ed7CAS | 22649059PubMed | open url image1

Volinia, S., Calin, G., Liu, C. G., Ambs, S., Cimmino, A., Petrocca, F., Visone, R., Iorio, M., Roldo, C., Ferracin, M., Prueitt, R. L., Yanaihara, N., Lanza, G., Scarpa, A., Vecchione, A., Negrini, M., Harris, C. C., and Croce, C. M. (2006). A microRNA expression signature in human solid tumors defines cancer targets. Proc. Natl Acad. Sci. USA 103, 2257–2261.
A microRNA expression signature in human solid tumors defines cancer targets.CrossRef | 1:CAS:528:DC%2BD28XhslGjsbg%3D&md5=5fc897d482e4d21db86be48e8eadc17eCAS | 16461460PubMed | open url image1

Voorhoeve, P. M., le Sage, C., Schrier, M., Gillis, A. J., Stoop, H., Nagel, R., Liu, Y. P., van Duijse, J., Drost, J., Griekspoor, A., Zlotorynski, E., Yabuta, N., De Vita, G., Nojima, H., Looijenga, L. H., and Agami, R. (2006). A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors. Cell 124, 1169–1181.
A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors.CrossRef | 1:CAS:528:DC%2BD28Xjt1Khsrg%3D&md5=93af690f0133b5c64804f2265818a8fcCAS | 16564011PubMed | open url image1

Wydooghe, E., Vandaele, L., Heras, S., De Sutter, P., Deforce, D., Peelman, L., De Schauwer, C., and Van Soom, A. (2015). Autocrine embryotropins revisited: how do embryos communicate with each other in vitro when cultured in groups? Biol. Rev. Camb. Philos. Soc. , .
Autocrine embryotropins revisited: how do embryos communicate with each other in vitro when cultured in groups?CrossRef | 26608222PubMed | open url image1

Xu, D., Takeshita, F., Hino, Y., Fukunaga, S., Kudo, Y., Tamakim, A., Matsunaga, J., Takahashi, R. U., Takata, T., Shimamoto, A., Ochiya, T., and Tahara, H. (2011). miR-22 represses cancer progression by inducing cellular senescence. J. Cell Biol. 193, 409–424.
miR-22 represses cancer progression by inducing cellular senescence.CrossRef | 1:CAS:528:DC%2BC3MXltlGjt7o%3D&md5=1b9b50d2e937a61f47dde6e17a5b3b9cCAS | 21502362PubMed | open url image1

Xue, J., Chen, Z., Gu, X., Zhang, Y., and Zhang, W. (2016). MicroRNA-148a inhibits migration of breast cancer cells by targeting MMP-13. Tumour Biol. 37, 1581–1590.
MicroRNA-148a inhibits migration of breast cancer cells by targeting MMP-13.CrossRef | 1:CAS:528:DC%2BC2MXhsVWgsbfJ&md5=df26770cf0fd3607e45c499ab31c9611CAS | 26298724PubMed | open url image1

Yang, Y., Bai, W., Zhang, L., Yin, G., Wang, X., Wang, J., Zhao, H., Han, Y., and Yao, Y. Q. (2008). Determination of microRNAs in mouse preimplantation embryos by microarray. Dev. Dyn. 237, 2315–2327.
Determination of microRNAs in mouse preimplantation embryos by microarray.CrossRef | 1:CAS:528:DC%2BD1cXhtFylsb%2FF&md5=53bf0631d9c29423f71d2a3cced85a59CAS | 18729214PubMed | open url image1



Rent Article (via Deepdyve) Supplementary MaterialSupplementary Material (409 KB) Export Citation

View Altmetrics